HYBRID ZONE DYNAMICS AND SPECIES REPLACEMENT BETWEEN ORCONECTES CRAYFISHES IN A NORTHERN WISCONSIN LAKE
William L. Perry
Behavioral, Evolution, Ecology, and Systematics Section, Department of Biological Sciences, Illinois State University, Campus Box 4120, Normal, Illinois 61790-4120 E-mail: [email protected]
Search for more papers by this authorJeffrey L. Feder
Department of Biological Sciences, University of Notre Dame, P.O. Box 369, Notre Dame, Indiana 46556-0369
Department of Biological Sciences, University of Notre Dame, P.O. Box 369, Notre Dame, Indiana 46556-0369. E-mail: [email protected]
Search for more papers by this authorGreg Dwyer
Department of Ecology and Evolution, Biological Sciences Collegiate Division, The University of Chicago, 5801 South Ellis, Chicago, Illinois 60637
Department of Ecology and Evolution, Biological Sciences Collegiate Division, The University of Chicago, 5801 South Ellis, Chicago, Illinois 60637. E-mail: [email protected]
Search for more papers by this authorDavid M. Lodge
Department of Biological Sciences, University of Notre Dame, P.O. Box 369, Notre Dame, Indiana 46556-0369
Department of Ecology and Evolution, Biological Sciences Collegiate Division, The University of Chicago, 5801 South Ellis, Chicago, Illinois 60637. E-mail: [email protected]
Search for more papers by this authorWilliam L. Perry
Behavioral, Evolution, Ecology, and Systematics Section, Department of Biological Sciences, Illinois State University, Campus Box 4120, Normal, Illinois 61790-4120 E-mail: [email protected]
Search for more papers by this authorJeffrey L. Feder
Department of Biological Sciences, University of Notre Dame, P.O. Box 369, Notre Dame, Indiana 46556-0369
Department of Biological Sciences, University of Notre Dame, P.O. Box 369, Notre Dame, Indiana 46556-0369. E-mail: [email protected]
Search for more papers by this authorGreg Dwyer
Department of Ecology and Evolution, Biological Sciences Collegiate Division, The University of Chicago, 5801 South Ellis, Chicago, Illinois 60637
Department of Ecology and Evolution, Biological Sciences Collegiate Division, The University of Chicago, 5801 South Ellis, Chicago, Illinois 60637. E-mail: [email protected]
Search for more papers by this authorDavid M. Lodge
Department of Biological Sciences, University of Notre Dame, P.O. Box 369, Notre Dame, Indiana 46556-0369
Department of Ecology and Evolution, Biological Sciences Collegiate Division, The University of Chicago, 5801 South Ellis, Chicago, Illinois 60637. E-mail: [email protected]
Search for more papers by this authorAbstract
Abstract.— Hybrid zones that result in the genetic assimilation (replacement) of one species by another are underrepresented in the animal literature, most likely due to their transient nature. One such zone involves the rusty crayfish, Orconectes rusticus, and its congener O. propinquus. Orconectes rusticus was recently introduced into northern Wisconsin and Michigan lakes and streams, where it is hybridizing with and displacing resident O. propinquus. Here we report on a study investigating the dynamics of a hybrid zone between the two crayfish in Trout Lake, Wisconsin, where both the time (circa 1979) and location of the initial introduction are known. Our prediction was that hybridization should hasten the demise of O. propinquus because we expected that male O. rusticus (which are larger than congeners) would outcompete male O. propinquus for mates of both species. If hybrid progeny are unfit, then the result would be decreased reproductive output of O. propinquus females. However, we found a pattern of cytonuclear disequilibrium between allozymes and mtDNA suggesting that a majority (94.5%) of F1 hybrids resulted from matings between O. rusticus females and O. propinquus males. Also contrary to expectations, fecundity (O. rusticus and O. propinquus) and early hybrid survivorship did not differ significantly from nonhybrids. Moreover, adults of mixed ancestry were superior to both O. rusticus and O. propinquus in competition for a limiting food resource. Using a single-locus model, we estimated that hybridization increases the advance of O. rusticus genes in Trout Lake between 4.8% and 36.3% above that due to the previously documented ecological interactions. Consequently, whereas hybridization may be hastening the elimination of genetically pure O. propinquus, introgression is nevertheless slowing the loss of O. propinquus nuclear genes. Although our results suggest that O. rusticus and O. propinquus may not be true species under the biological concept, their ecological differences are of great conservation importance.
Literature Cited
- Arnold, M. L. 1997. Natural hybridization and evolution. Pp. 1–215 in R. M. May and P. H. Harvey, eds. Oxford series in ecology and evolution. Oxford Univ. Press, New York .
- Asmussen, M. A., and C. J. Basten. 1994. Sampling theory for cytonuclear disequilibria. Genetics 138: 1351–1363.
- Avise, J. C., E. Bermingham, L. G. Kessler, and N. C. Saunders. 1984. Characterization of mitochondrial DNA variability in a hybrid swarm between subspecies of bluegill sunfish (Lepomis macrochirus). Evolution 38: 931–941.
- Berrill, M. 1978. Distribution and ecology of crayfish in the Kawartha Lakes region of southern Ontario. Can. J. Zool. 56: 166–177.
- Brochman, C. 1984. Hybridization distribution of Argyranthemum coronopifolium (Asteraceae, Anthemideae) in the Canary Islands (Spain). Nordic J. Bot. 4: 729–736.
- Brown, K. 1981. Low genetic variability and high similarities in the crayfish genera Cambarus Procambarus. Am. Midl. Nat. 105: 225–232.
- Butler, M. J. 1988. Evaluation of possible reproductively mediated character displacement in the caryfishes, Orconectes rusticus and Orconectes sanbornii. Ohio J. Sci. 88: 87–91.
- Butler, M. J., and R. A. Stein. 1985. An analysis of the mechanisms governing species replacements in crayfish. Oecologia 66: 168–177.
- Capelli, G. M. 1975. Distribution, life history, and ecology of crayfish in northern Wisconsin, with emphasis on Orconectes propinquus. Ph.D. diss., Univ. of Wisconsin, Madison, WI.
- Capelli, G. M., and J. F. Capelli. 1980. Hybridization between crayfish of the genus Orconectes: morphological evidence (Decapoda, Cambaridae). Crustaceana 39: 121–132.
- Capelli, G. M., and J. H. Magnuson. 1983. Morphoedaphic and biogeographic analysis of crayfish distribution in northern Wisconsin. J. Crust. Biol. 3: 548–564.
- Capelli, G. M., and B. L. Munjal. 1982. Aggressive interactions and resource competition in relation to species displacement among crayfish of the genus Orconectes. J. Crust. Biol. 2: 486–492.
- Childs, M. R., A. A. Echelle, and T. E. Dowling. 1996. Development of the hybrid swarm between pecos pupfish (Cyprinodontidae: Cyprinodon pecosensis) and sheepshead minnow (Cyprinodon variegatus): a perspective from allozymes mtDNA. Evolution 50: 2014–2022.
- Corey, S. 1987a. Comparative fecundity of four species of crayfish in southwestern Ontario, Canada (Decapoda, Astacidea). Crustaceana 52: 276–286.
- Corey, S. 1987b. Intraspecific differences in reproductive potential, realized reproduction and actual production in the crayfish Orconectes propinquus (Girard) in Ontario. Am. Midl. Nat. 118: 424–432.
- Cracraft, J. 1989. Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. Pp. 28–59 in D. Otte and J. A. Endler, eds. Speciation and its consequences. Sinauer Associates, Inc., Sunderland , MA .
- Daehler, C. C., and D. R. Strong. 1997. Hybridization between introduced smooth cordgrass (Spartina alterniflora; Poaceae) and native California cordgrass (S. foliosa) in San Francisco Bay, California, USA. Am. J. Bot. 84: 607–611.
- DiDonato, G. W., and D. M. Lodge. 1993. Species replacements among Orconectes crayfishes in Wisconsin lakes: the role of predation by fish. Can. J. Fish. Aquat. Sci. 50: 1484–1488.
- Dowling, T. E., and M. R. Childs. 1992. Impact of hybridization on a threatened trout of the southwestern United States. Conserv. Biol. 6: 355–364.
-
Dunham, R. A.,
C. J. Turner, and
W. C. Reeves. 1992. Introgression of the Florida largemouth bass genome into native populations in Alabama public lakes.
N. Am. J. Fish. Manage.
12: 494–498.
10.1577/1548-8675(1992)012<0494:IOTFLB>2.3.CO;2 Google Scholar
- Echelle, A. A., and A. F. Echelle. 1997. Genetic introgression of endemic taxa by non-natives; a case study involving Leon springs pupfish and sheepshead minnow. Conserv. Biol. 11: 1–9.
- Fasten, N. 1914. Spermatogenesis of the American crayfish, Cambarus virilis and C. immunis, with special reference to synapsis and the chromatoid bodies. J. Morphol. 25: 587–649.
- Fisher, R. A. 1937. The wave of advance of advantageous genes. Ann. Eugen. 7: 355–369.
- Garvey, J. E., and R. A. Stein. 1993. Evaluating how chela size influences the invasion potential of an introduced crayfish (Orconectes rusticus). Am. Midl. Nat. 129: 172–181.
- Garvey, J. E., R. A. Stein, and H. T. Thomas. 1994. Assessing how fish predation and interspecific prey competition influence a crayfish assemblage. Ecology 75: 532–547.
- Gill, F. B. 1997. Local cytonuclear extinction of the golden-winged warbler. Evolution 51: 519–525.
-
Gill, F. B.
1998. Hybridization in birds.
Auk
115: 282–283.
10.2307/4089187 Google Scholar
-
Harrison, R. G.
1993. Hybrid zones and the evolutionary process. Oxford Univ. Press,
New York
.
10.1093/oso/9780195069174.001.0001 Google Scholar
- Hewitt, G. M. 1988. Hybrid zones: natural laboratories for evolutionary studies. Trends Ecol. Evol. 3: 158–167.
- Hill, A. M., and D. M. Lodge. 1994. Diel changes in resource demand: competition and predation in species replacement among crayfishes. Ecology 75: 2118–2126.
- Hill, A. M., and D. M. Lodge. 1995. Multi-trophic-level impact of sublethal interactions between bass and omnivorous crayfish. J. N. Am. Benthol. Soc. 14: 306–314.
- Hill, A. M., and D. M. Lodge. 1999. Replacement of resident crayfishes by an exotic crayfish: the roles of competition and predation. Ecol. Appl. 9: 678–690.
- Hill, A. M., D. M. Sinars, and D. M. Lodge. 1993. Invasion of an occupied niche by the crayfish Orconectes rusticus: potential importance of growth and mortality. Oecologia 94: 303–306.
- Hobbs, H. H., III, and J. P. Jass. 1988. The crayfishes and shrimps of Wisconsin. Milwaukee Public Museum, Milwaukee , WI .
-
Howard, D. J.
1993. Reinforcement: origin, dynamics, and fate of an evolutionary hypothesis. Pp.
46–69
in
R. G. Harrison, ed.
Hybrid zones and the evolutionary process. Oxford Univ. Press,
New York
.
10.1093/oso/9780195069174.003.0003 Google Scholar
- Kershner, M. W., and D. M. Lodge. 1995. Effects of littoral habitat and fish predation on the distribution of an exotic crayfish, Orconectes rusticus. J. N. Am. Benthol. Soc. 14: 414–422.
- Kot, M., M. A. Lewis, and P. van den Driessche. 1996. Dispersal data and the spread of invading organisms. Ecology 77: 2027–2042.
- Levin, D. A., J. Francisco-Ortega, and R. K. Jansen. 1996. Hybridization and the extinction of rare plant species. Conserv. Biol. 10: 10–16.
- Lodge, D. M. 2001. Lakes. In O. E. Sala, F. S. Chapin, and E. Huber-Sannwald, eds. Future scenarios of global biodiversity. Springer-Verlag, Berlin . In press.
- Lodge, D. M., and J. G. Lorman. 1987. Reductions in submersed macrophyte biomass species richness by the crayfish Orconectes rusticus. Can. J. Fish. Aquat. Sci. 44: 591–597.
- Lodge, D. M., A. L. Beckel, and J. J. Magnuson. 1985. Lake-bottom tyrant. Nat. Hist. 8: 133–137.
- Lodge, D. M., T. K. Kratz, and G. M. Capelli. 1986. Long-term dynamics of three crayfish species in Trout Lake, Wisconsin (USA). Can. J. Fish. Aquat. Sci. 43: 993–998.
- Lodge, D. M., M. W. Kershner, J. E. Aloi, and A. P. Covich. 1994. Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web. Ecology 75: 1265–1281.
- Lodge, D. M., R. A. Stein, K. W. Brown, A. P. Covich, C. Brönmark, J. E. Garvey, and S. P. Klosiewski. 1998. Predicting impact of freshwater exotic species on native biodiversity: challenges in spatial scaling. Aust. J. Ecol. 23: 53–67.
- Lodge, D. M., C. A. Taylor, D. M. Holdich, and J. Skurdal. 2000. Nonindigenous crayfishes threaten North American freshwater biodiversity: lessons from Europe. Fisheries 25: 7–19.
- Lorman, J. G. 1980. Ecology of the crayfish Orconectes rusticus in northern Wisconsin. Ph.D. diss., University of Wisconsin, Madison.
- Lorman, J. G., and J. J. Magnuson. 1978. The role of crayfishes in aquatic ecosystems. Fisheries 3: 8–10.
- Magnuson, J. J., G. M. Capelli, J. G. Lorman, and R. A. Stein. 1975. Consideration of crayfish for macrophyte control. Pp. 66–74 in P. L. Brezonik and J. L. Fox eds. The proceedings of a symposium on water quality management through biocontrol. Rep. no. ENV 07–75–1, Univ. of Florida, Gainsville .
- Mallet, J. 1995. A species definition for the modern synthesis. Trends Ecol. Evol. 10: 294–299.
-
Mayr, E.
1963. Animal species and evolution. Harvard Univ. Press,
Cambridge
,
MA
.
10.1111/j.0022-1112.2004.00433.x Google Scholar
- Momot, W. T. 1992. Further range extensions of the crayfish Orconectes rusticus in the Lake Superior Basin of northwestern Ontario. Can. Field Nat. 106: 397–399.
- Murofushi, M., T. Nakatubo, and Y. Deguchi. 1990. Karyotype analysis of the red swamp crayfish Procambarus clarkii by cell culture. Abstract no. 111 in Third international Crustacean Conference, The University of Queensland, Brisbane , Australia .
- Murphy, R. W., J. W. Sites Jr., D. G. Buth, and C. H. Haufler. 1990. Proteins I: isozyme electrophoresis. Pp. 45–126 in D. M. Hillis and C. Moritz, eds. Molecular systematics. Sinauer Associates, Sunderland , MA .
-
Murray, J. D.
1989. Mathematical biology. Springer-Verlag,
Berlin
.
10.1007/978-3-662-08539-4 Google Scholar
- Nason, J. D., and N. C. Ellstrand. 1993. Estimating the frequencies of genetically distinct classes of individuals in hybridized populations. J. Hered. 84: 1–12.
- Niiyama, H. 1934. The chromosome number of the crayfish Cambaroides japonicus (de Haan). J. Fac. Sci. Hokkaido Imp. Univ. Ser. VI., Zoology 3: 41–53.
- Noor, M. A. 1995. Speciation driven by natural selection in Drosophila. Nature 375: 674–675.
- Okubo, A. 1980. Diffusion and ecological problems: mathematical models. Series Biomathematics vol. 10. Springer-Verlag, New York .
- Olsen, T. M., D. M. Lodge, G. M. Capelli, and R. J. Houlihan. 1991. Mechanisms of impact of an introduced crayfish (Orconectes rusticus) on littoral congeners, snails, and macrophytes. Can. J. Fish. Aquat. Sci. 48: 1853–1861.
- Page, L. M. 1985. The crayfishes shrimps (Decapoda) of Illinois. Illinois Natural History Survey Bulletin no. 33.
- Perry, W. L., J. L. Feder, and D. M. Lodge. 2001. Hybridization and introgression between introduced and resident Orconectes crayfishes. Conserv. Biol. In press.
- Pipas, J. C., and F. J. Bulow. 1998. Hybridization between redeye bass and smallmouth bass in Tennessee streams. Trans. Am. Fish. Soc. 127: 141–146.
-
Rhymer, J. M., and
D. Simberloff. 1996. Extinction by hybridization and introgression.
Annu. Rev. Ecol. Syst.
27: 83–109.
10.1146/annurev.ecolsys.27.1.83 Google Scholar
- Rieseberg, L. H., and D. Gerber. 1995. Hybridization in the Catalina Island mountain mahogany (Cercocarpus traskiae): RAPD evidence. Conserv. Biol. 9: 199–203.
-
Rieseberg, L. H., and
J. Wendel. 1993. Introgression and its consequences in Plants. Pp.
70–114
in
R. Harrison, ed.
Hybrid zones and the evolutionary process. Oxford University Press,
New York
.
10.1093/oso/9780195069174.003.0004 Google Scholar
- Rieseberg, L. H., S. Zona, L. Aberbom, and T. D. Martin. 1989. Hybridization in the island endemic, Catalina mahogany. Conserv. Biol. 3: 52–58.
- Roche, C. T., and B. F. J. Roche. 1991. Meadow knapweed invasion in the Pacific Northwest, USA, British Columbia, Canada. Northwest Sci. 65: 53–61.
- Sala, O. E., F.S. Chapin III, J. J. Armesto, E. Berlow, J. Bloomfield, R. Dirzo, E. Huber-Sannwald, L. Huenneke, R. B. Jackson, A. Kinzig, R. Leemans, D. M. Lodge, H. A. Mooney, M. Oesterheld, N. L. Poff, M. T. Sykes, B. H. Walker, M. Walker, and D. H. Wall. 2000. Biodiversity scenarios for the year 2100. Science 287: 1770–1774.
-
Sambrook, J.,
E. F. Fritsch, and
T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Press,
Cold Spring Harbor
,
NY
.
10.1111/j.1095-8312.1996.tb01434.x Google Scholar
- Shapiro, L. H. 1998. Hybridization and geographic variation in two meadow katydid contact zones. Evolution 52: 784–796.
- Simon, C., F. Frati, A. Beckenbach, B. Crespi, H. Liu, P. Flook. 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87: 651–701.
- Snedden, W. A. 1990. Determinants of male mating success in the temperate crayfish Orconectes rusticus: chela size and sperm competition. Behaviour 115: 100–113.
- Taylor, C. A., and M. Redmer. 1996. Dispersal of the crayfish Orconectes rusticus in Illinois, with notes on species displacement and habitat preference. J. Crust. Biol. 16: 547–551.
- Taylor, C. A., M. L. Warren Jr., J. F. Fitzpatrick, H. H. Hobbs III, R. F. Jezerinac, W. L. Pflieger, and H. W. Robison. 1996. Conservation status of crayfishes of the United States. Fisheries 21: 25–28.
- Tierney, A. J., and D. W. Dunham. 1984. Behavioral mechanisms of reproductive isolation in crayfishes of the genus Orconectes. Am. Midland Nat. 111: 304–310.
- Williams, R. N., D. K. Shiozawa, J. E. Carter, and R. F. Leary. 1996. Genetic detection of putative hybridization between native and introduced rainbow trout populations of the Upper Snake River. Trans. Am. Fish. Soc. 125: 387–401.
